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University of Copenhagen, Denmark Impact and control of protozoan parasites in maricultured fishes Buchmann, Kurt Published in: Parasitology DOI: 10.1017/S003118201300005X Publication date: 2015 Document version Early version, also known as pre-print Citation for published version (APA): Buchmann, K. (2015). Impact and control of protozoan parasites in maricultured fishes. Parasitology, 142(special issue 01), 168-177. https://doi.org/10.1017/S003118201300005X Download date: 27. Sep. 2021 168 Impact and control of protozoan parasites in maricultured fishes KURT BUCHMANN* Laboratory of Aquatic Pathobiology, Section of Biomedicine, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark (Received 14 November 2012; revised 8 January 2013; accepted 8 January 2013; first published online 1 March 2013) SUMMARY Aquaculture, including both freshwater and marine production, has on a world scale exhibited one of the highest growth rates within animal protein production during recent decades and is expected to expand further at the same rate within the next 10 years. Control of diseases is one of the most prominent challenges if this production goal is to be reached. Apart from viral, bacterial, fungal and metazoan infections it has been documented that protozoan parasites affect health and welfare and thereby production of fish in marine aquaculture. Representatives within the main protozoan groups such as amoebae, dinoflagellates, kinetoplastid flagellates, diplomonadid flagellates, apicomplexans, microsporidians and ciliates have been shown to cause severe morbidity and mortality among farmed fish. Well studied examples are Neoparamoeba perurans, Amyloodinium ocellatum, Spironucleus salmonicida, Ichthyobodo necator, Cryptobia salmositica, Loma salmonae, Cryptocaryon irritans, Miamiensis avidus and Trichodina jadranica. The present report provides details on the parasites’ biology and impact on productivity and evaluates tools for diagnosis, control and management. Special emphasis is placed on antiprotozoan immune responses in fish and a strategy for development of vaccines is presented. Key words: fish, parasites, protozoans, health, productivity, impact, vaccine, control. INTRODUCTION chemical/medical intervention and immunoprophy- laxis including vaccination, which is currently used Production of teleosts in the marine environment is a for control of bacterial diseases. Metazoan parasites rapidly developing aquacultural activity worldwide. including helminths and crustaceans are also con- In relation to the known number of fish species sidered severe pests in mariculture enterprises and described, which counts more than 28000 species these parasites are in many cases visible to the naked (Nelson, 2006), relatively few of these (< 400 species) eye and therefore easily diagnosed disease agents. are currently being propagated under artificial con- Protozoans are limited in size and more difficult to ditions. However, even on this constricted basis, diagnose. If infections are observed macroscopically production of marine fish in aquaculture enterprises this will be due to pathological tissue changes is a prominent player on the world market. In 2010, (hyperplasia, hypertrophy or necrosis of host tissue) the Atlantic salmon (Salmo salar) was produced in induced by the protozoans. Despite the limited size of quantities of more than 1.5 million tonnes, milkfish protozoans their pathogenic effects on fish may be (Chanos chanos) production exceeded 0.8 million devastating and can negatively impact on fish pro- tonnes and sea bass (Dicentrarchus labrax) and sea duction. The present report provides examples of bream (Sparus aurata) rearing reached more than problems in marine fish farming caused by amoebae, 450000 tonnes (FAO, 2012). As in all other types of flagellates, apicomplexans, microsporideans and husbandry, infectious diseases represent one of the ciliates. main obstacles for safe production securing a high level of animal welfare (Rodgers and Furones, 1998; Segner et al. 2012). Viral, bacterial and fungal diseases represent well known challenges to mari- AMOEBAE culture enterprises and call for special methods for Neoparamoeba perurans successful control. Strategies rely on improved management procedures, breeding of resistant fish, Salmon farming in Tasmania, Europe, South America and North America suffers from infections with amoebae of the species Neoparamoeba perurans, * Corresponding author: Laboratory of Aquatic a parasite causing amoebic gill disease (AGD) in Pathobiology, Section of Biomedicine, Department of Atlantic salmon (S. salar) in marine fish farms Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Stigbøjlen (Young et al. 2007; Rozas et al. 2012). It is one of 7, DK-1870 Frederiksberg C., Denmark. Tel: +45- the best documented gill diseases in salmon farming 35332700. Fax: +45-35332755. E-mail: [email protected] eliciting high morbidity and some mortality. Other Parasitology (2015), 142, 168–177. © Cambridge University Press 2013 doi:10.1017/S003118201300005X Protozoan parasites in mariculture 169 species of Neoparamoeba have been isolated from PCR and sequencing of rDNA have been developed various marine fishes (Dyková et al. 2007) but only (Levy et al. 2007). The pathogenic effect of the para- N. perurans has been proven explicitly to elicit site is associated with severe disturbance of epithelia pathological reactions in fish gills (Young et al. which evidently can lead to osmoregulatory problems 2008). Apart from Atlantic salmon host fishes such in the host fish (Noga, 1987). Effective treatment of as coho salmon (Oncorhynchus kisutch), chinook infections has been achieved by use of auxiliary salmon (O. tshawytscha), rainbow trout (O. mykiss), compounds containing formalin, copper and hydro- ayu (Plecoglossus altivelis), sea bass (D. labrax) and gen peroxide, but experimental trials have shown that turbot (Scophthalmus maximus) have been diagnosed also drugs such as chloroquine chloride and a series of with AGD (Nowak, 2012). Amoebae induce hyper- antibiotics have effects on A. ocellatum infections in plasia in affected gill areas where inflammatory foci, fish (Noga, 2012). Epithelial sloughing and rhizoid clubbing and filament fusion may occur. Diagnosis penetration will presumably activate a series of im- requires use of molecular tools (PCR or in situ mune reactions which have not been fully described hybridization) because light microscopy cannot but the severe hyperplasia and inflammatory reac- differentiate between e.g. genera Paramoeba and tions elicited by the parasites are probably associated Neoparamoeba, both carrying eukaryotic endosym- with extensive production of cytokines. A series of bionts. Neoparamoeba perurans is a marine species antimicrobial peptides such as HLPs (histone-like and treatment can be performed by freshwater proteins) and piscidins produced in the skin of certain bathing but use of hydrogen peroxide treatments fish species show a clear killing effect on dinospores. have shown some effects as well (Nowak, 2012). It has also been shown that specific serum antibodies Irritation of gill epithelia following invasion by occur in hosts following infection and recovery amoebae lead to IL-1beta expression followed by (Smith et al. 1992; Cecchini et al. 2001) which at hyperplasia (Adams and Nowak, 2003) and higher least could partly explain the dinospore-agglutinating infections lead to extensive inflammatory responses activity of tilapia serum (Smith et al. 1993). Clown with infiltration of reactive cells. These reactions fish (Amphiprion frenatus) surviving from experi- clearly indicate that host immune responses are mental infections developed acquired immunity to activated following infection but also that they are reinfection lasting for half a year (Cobb et al. 1998) part of the pathological reactions destroying the which suggest that development of a protective architecture of the gill tissue leading to decreased vaccine may be a realistic future goal. oxygen uptake and carbon dioxide release (Nowak, 2012). Control strategies may include breeding for Ichthyodinium spp. resistant salmon strains but immunoprophylactic measures should be considered as well. Feeding The endoparasitic dinoflagellate Ichthyodinium was salmon with immunostimulating feed additives, previously known from wild fish and fish eggs but which often has been suggested to boost the fish following the advent of cod (Gadus morhua) farming immune system, did not show a satisfactory effect on (Buchmann et al. 1993; Pedersen et al. 1993) fish and infection levels (Bridle et al. 2005). Vaccines (im- eggs from these marine species were found to be infec- mersion or injection) based on live or killed amoebae ted by dinoflagellates during routine investigations and even DNA vaccines have been tested experimen- for diseases and a tentative diagnosis based on light tally but without showing any significant efficacy microscopy was made. However, a precise generic (Nowak, 2012). diagnosis was only recently obtained following sequencing of rDNA from the organism (Skovgaard DINOFLAGELLATES et al. 2010). The parasite occurs as a trophozoite in eggs and yolk sac larvae and it was initially suggested Amyloodinium ocellatum that infection could affect host survival, a suggestion, The dinoflagellate A. ocellatum has an ectoparasitic however, that could not be confirmed by Skovgaard life style and has been considered a pest in marine et al. (2010). The absence of multiplication in eggs aquaculture for decades due
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